Complex Bifurcation Structures in the Hindmarsh–Rose Neuron Model
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International Journal of Bifurcation and Chaos, Vol. 17, No. 9 (2007) 3071–3083 c World Scientific Publishing Company COMPLEX BIFURCATION STRUCTURES IN THE HINDMARSH–ROSE NEURON MODEL J. M. GONZALEZ-MIRANDA´ Departamento de F´ısica Fundamental, Universidad de Barcelona, Avenida Diagonal 647, Barcelona 08028, Spain Received June 12, 2006; Revised October 25, 2006 The results of a study of the bifurcation diagram of the Hindmarsh–Rose neuron model in a two-dimensional parameter space are reported. This diagram shows the existence and extent of complex bifurcation structures that might be useful to understand the mechanisms used by the neurons to encode information and give rapid responses to stimulus. Moreover, the information contained in this phase diagram provides a background to develop our understanding of the dynamics of interacting neurons. Keywords: Neuronal dynamics; neuronal coding; deterministic chaos; bifurcation diagram. 1. Introduction 1961] has proven to give a good qualitative descrip- There are two main problems in neuroscience whose tion of the dynamics of the membrane potential of solution is linked to the research in nonlinear a single neuron, which is the most relevant experi- dynamics and chaos. One is the problem of inte- mental output of the neuron dynamics. Because of grated behavior of the nervous system [Varela et al., the enormous development that the field of dynam- 2001], which deals with the understanding of the ical systems and chaos has undergone in the last mechanisms that allow the different parts and units thirty years [Hirsch et al., 2004; Ott, 2002], the of the nervous system to work together, and appears study of meaningful mathematical systems like the related to the synchronization of nonlinear dynami- Hindmarsh–Rose model have acquired new interest cal oscillators. The other is the neural coding prob- [Holmes, 2005] because of the new information that can now be obtained from them. Int. J. Bifurcation Chaos 2007.17:3071-3083. Downloaded from www.worldscientific.com lem [Sejnowski, 1995; Abeles, 2004], which is aimed to know how the neurons encode the information In particular, it has been found recently that that they transmit and exchange in the working the dynamics of this system, when studied as a of the nervous system, and is related to both, the function of significant control parameters, presents knowledge of the different types of dynamics avail- two relevant features: (i) continuous interior cri- able to nonlinear dynamical systems and to chaos sis [Gonz´alez-Miranda, 2003], which are abrupt synchronization. changes in the nature of the dynamics of the sys- The theoretical study of such problems, in its tem attractor, and (ii) block structured dynamics by SOUTH CHINA UNIVERSITY OF TECHNOLOGY on 01/01/19. Re-use and distribution is strictly not permitted, except for Open Access articles. most basic aspects, partly relies on mathematical [Gonz´alez-Miranda, 2005], which is a complex bifur- models of the electrophysics of a single neuron, cation structure where the dynamics available to the most of them developed from the pioneering work system are grouped in blocks of alike periodicity. by Hodgkin and Huxley [1952]. Among them, the The first of these items provides a potential mech- model by Hindmarsh and Rose [1984], which is the anism for rapid responses in the nervous system result of a mapping of the Hodgkin–Huxley model by switching between different dynamical behav- to a relatively simple nonlinear oscillator [Fitzhugh, iors. The second provides structures that appear as 3071 3072 J. M. Gonz´alez-Miranda possible basic elements to encode messages in the 1.5 apparently random trains of action potentials that x run along the axon of an activated neuron. 0 -1.5 These two phenomena have received detailed study at particular restricted values of the 1.5 Hindmarsh–Rose model parameters. The aim of the x 0 present paper is to report a comprehensive study of -1.5 the manifestation of these phenomena for a wide 1.5 range of system parameters; that is, to provide x 0 a phase diagram of the Hindmarsh–Rose model, -1.5 which gives a global view of the availability of these 1.5 and other dynamical behaviors to this system. x This article is arranged as follows. After this 0 introduction, in Sec. 2, we give a basic description -1.5 of the complexities in the bifurcation diagrams of 1.5 the Hindmarsh–Rose neuron model. In Sec. 3, we x 0 present the results of a linear stability analysis in a -1.5 wide and significant region of the parameter space. 1.5 In Sec. 4, we analyze stability from the nonlinear x 0 point of view by means of the use of Lyapunov -1.5 exponents, and go further in the nonlinear analy- 1.5 sis giving a global view of the bifurcation diagrams. x In Sec. 5, we provide evidence for the structural sta- 0 bility of the above results, and finally, in Sec. 6 we -1.5 0 200 400 600 800 1000 1200 discuss and summarize the main conclusions of the t paper. Fig. 1. Time series for the action potential for the Hindmarsh–Rose model for r =0.003 and different values of 2. Complex Bifurcation Structures the current applied: (a) I =1.26, (b) I =1.28, (c) I =1.67, (d) I =3.20, (e) I =3.29, (f) I =3.34, and (g) I =3.50. The Hindmarsh–Rose model describes the dynam- ics of the membrane potential in the axon of a neu- ron, x(t), by means of a three-dimensional system oscillatory solutions than can be simple periodic fir- of nonlinear first-order differential equations, which ings of a single spike [Figs. 1(b) and 1(g)], periodic written in dimensionless form read: firings of well-defined bursts of spikes [Figs. 1(c) and 1(d)], or chaotic firings of spikes and bursts of x˙ = y +3x2 − x3 − z + I, (1) spikes [Figs. 1(f) and 1(e)]. Most of these dynam- Int. J. Bifurcation Chaos 2007.17:3071-3083. Downloaded from www.worldscientific.com 2 ical behaviors being oscillatory, they can be char- y˙ =1− 5x − y, (2) acterized by means of the time intervals between 8 consecutive peaks, Ti (i =1, 2,...,N), for each z˙ = r 4 x + − z . (3) 5 function x(t). In neurobiology, these time inter- vals, Ti, are known as inter-spike intervals, and it is The other two dynamical variables, y(t)andz(t), believed that in the structure of inter-spike intervals describe the exchange of ions through the neuron is where neurons encode the information [Sejnowski, by SOUTH CHINA UNIVERSITY OF TECHNOLOGY on 01/01/19. Re-use and distribution is strictly not permitted, except for Open Access articles. membrane by means of fast and slow ion channels, 1995; Abeles, 2004]. Therefore, they are the relevant respectively. The main parameters of the model are observables for neuronal dynamics; because of this, the current that enters the neuron, I,andtheeffi- they will be our basic observables here. ciency of the slow channels to exchange ions, r. We have used them to construct one- The dynamics that one can observe for the dimensional bifurcation diagrams as those pre- action potential, x(t), are quite diverse as illus- sented in Fig. 2. These have been obtained through trated in Fig. 1. There are equilibrium solutions the numerical integration of the equations of where the action potential decays to a constant motion, Eqs. (1)–(3), by means of a fourth-order value, as shown in Fig. 1(a), as well as a variety of Runge–Kutta algorithm with time step 0.005. The Complex Bifurcation Structures 3073 (a) (b) Fig. 2. Two examples of bifurcation diagrams computed for different bifurcation parameters: (a) for I changing and r fixed (r =0.003), and (b) for r changing and I fixed (I =3.25). A vertical dashed line signals the point where the continuous interior crisis occurs, and vertical dotted lines separate the blocks, identified by its periodicity number, p. For (b) only a selected set of blocks of low periodicity have been signaled to avoid having the figure cluttered up with dotted lines. value of one of the system parameters, r or I,was bursts of spikes are separated by lapses of qui- fixed, and time series solutions were obtained for a escence [Fig. 1(e)]. The dynamics in the spiking set of different values of the other parameter, which regime is characterized by one time scale, that of is considered a bifurcation parameter. Then, plot- the spikes, while in the bursting regime there are ting as dots the different values of Ti obtained for two time scales, one for the bursts and other for the each of the values given to the bifurcation param- spikes. The transition between these two dynami- eter, the bifurcation diagrams were obtained. We cal regimes is what is called a continuous interior will note that the conclusions that follow would crisis. For a detailed qualitative and quantitative had been the same if more conventional observables study of the these crisis the reader is referred to to construct the bifurcation diagrams, such as the [Gonz´alez-Miranda, 2003]. maxima of x(t) or the times of crossing a surface in Block structured dynamics is observed to the phase space, had been used. left of the bifurcation diagram, for 1.28 ≤ I ≤ 3.31. Representative results of what is obtained for In this case the dynamical behaviors available can fixed r, and taking I as bifurcation parameter be classified in blocks accordingly to its period- appear in Fig. 2(a). In this case, the value of r is icity, p.